From thought to action: the parietal cortex as a bridge between perception, action, and cognition

The lateral intraparietal area (LIP) is a subdivision of the inferior parietal lobe that has been implicated in the guidance of spatial attention. In a variety of tasks, LIP provides a "salience representation" of the external world-a topographic visual representation that encodes the locations of salient or behaviorally relevant objects. Recent neurophysiological experiments show that this salience representation incorporates information about multiple behavioral variables-such as a specific motor response, reward, or category membership-associated with the task-relevant object. This integration occurs in a wide variety of tasks, including those requiring eye or limb movements or goal-directed or nontargeting operant responses. Thus, LIP acts as a multifaceted behavioral integrator that binds visuospatial, motor, and cognitive information into a topographically organized signal of behavioral salience. By specifying attentional priority as a synthesis of multiple task demands, LIP operates at the interface of perception, action, and cognition.     

Attentional modulations related to spatial gating but not to allocation of limited resources in primate V1

Attention can modulate neural responses in sensory cortical areas and improve behavioral performance in perceptual tasks. However, the nature and purpose of these modulations remain under debate. Here we?used voltage-sensitive dye imaging (VSDI) to measure V1 population responses while monkeys performed a difficult detection task under focal or distributed attention. We found that V1 responses at attended locations are significantly elevated relative to actively ignored or irrelevant locations, consistent with the hypothesis that an important goal of attention in V1 is to highlight task-relevant information. Surprisingly, these modulations were indistinguishable under focal and distributed attention, suggesting a minor or no role for attention as a mechanism for allocating limited representational resources in V1. The response elevation at attended locations is additive, is widespread, and starts shortly before stimulus onset. This elevation could contribute to spatial gating by biasing competition in subsequent processing stages in favor of attended stimuli.     

Spatial learning and action planning in a prefrontal cortical network model

The interplay between hippocampus and prefrontal cortex (PFC) is fundamental to spatial cognition. Complementing hippocampal place coding, prefrontal representations provide more abstract and hierarchically organized memories suitable for decision making. We model a prefrontal network mediating distributed information processing for spatial learning and action planning. Specific connectivity and synaptic adaptation principles shape the recurrent dynamics of the network arranged in cortical minicolumns. We show how the PFC columnar organization is suitable for learning sparse topological-metrical representations from redundant hippocampal inputs. The recurrent nature of the network supports multilevel spatial processing, allowing structural features of the environment to be encoded. An activation diffusion mechanism spreads the neural activity through the column population leading to trajectory planning. The model provides a functional framework for interpreting the activity of PFC neurons recorded during navigation tasks. We illustrate the link from single unit activity to behavioral responses. The results suggest plausible neural mechanisms subserving the cognitive "insight" capability originally attributed to rodents by Tolman & Honzik. Our time course analysis of neural responses shows how the interaction between hippocampus and PFC can yield the encoding of manifold information pertinent to spatial planning, including prospective coding and distance-to-goal correlates.     

Priorities for selection and representation in natural tasks

Selecting and remembering visual information is an active and competitive process. In natural environments, representations are tightly coupled to task. Objects that are task-relevant are remembered better due to a combination of increased selection for fixation and strategic control of encoding and/or retaining viewed information. However, it is not understood how physically manipulating objects when performing a natural task influences priorities for selection and memory. In this study, we compare priorities for selection and memory when actively engaged in a natural task with first-person observation of the same object manipulations. Results suggest that active manipulation of a task-relevant object results in a specific prioritization for object position information compared with other properties and compared with action observation of the same manipulations. Experiment 2 confirms that this spatial prioritization is likely to arise from manipulation rather than differences in spatial representation in real environments and the movies used for action observation. Thus, our findings imply that physical manipulation of task relevant objects results in a specific prioritization of spatial information about task-relevant objects, possibly coupled with strategic de-prioritization of colour memory for irrelevant objects.     

Competing sound sources reveal spatial effects in cortical processing

Why is spatial tuning in auditory cortex weak, even though location is important to object recognition in natural settings? This question continues to vex neuroscientists focused on linking physiological results to auditory perception. Here we show that the spatial locations of simultaneous, competing sound sources dramatically influence how well neural spike trains recorded from the zebra finch field L (an analog of mammalian primary auditory cortex) encode source identity. We find that the location of a birdsong played in quiet has little effect on the fidelity of the neural encoding of the song. However, when the song is presented along with a masker, spatial effects are pronounced. For each spatial configuration, a subset of neurons encodes song identity more robustly than others. As a result, competing sources from different locations dominate responses of different neural subpopulations, helping to separate neural responses into independent representations. These results help elucidate how cortical processing exploits spatial information to provide a substrate for selective spatial auditory attention.     

Hippocampal place cells demand attention

Hippocampal representations of the environment are thought to play a fundamental role in the encoding, storage, and retrieval of declarative memory. In this issue of Neuron, Kentros and coworkers show that new hippocampal representations stabilize only when animals are attentive.     

Visuospatial Tasks Affect Locomotor Control More than Nonspatial Tasks in Older People

Background

Previous research has shown that visuospatial processing requiring working memory is particularly important for balance control during standing and stepping, and that limited spatial encoding contributes to increased interference in postural control dual tasks. However, visuospatial involvement during locomotion has not been directly determined. This study examined the effects of a visuospatial cognitive task versus a nonspatial cognitive task on gait speed, smoothness and variability in older people, while controlling for task difficulty.

Methods

Thirty-six people aged ≥75 years performed three walking trials along a 20 m walkway under the following conditions: (i) an easy nonspatial task; (ii) a difficult nonspatial task; (iii) an easy visuospatial task; and (iv) a difficult visuospatial task. Gait parameters were computed from a tri-axial accelerometer attached to the sacrum. The cognitive task response times and percentage of correct answers during walking and seated trials were also computed.

Results

No significant differences in either cognitive task type error rates or response times were evident in the seated conditions, indicating equivalent task difficulty. In the walking trials, participants responded faster to the visuospatial tasks than the nonspatial tasks but at the cost of making significantly more cognitive task errors. Participants also walked slower, took shorter steps, had greater step time variability and less smooth pelvis accelerations when concurrently performing the visuospatial tasks compared with the nonspatial tasks and when performing the difficult compared with the easy cognitive tasks.

Conclusions

Compared with nonspatial cognitive tasks, visuospatial cognitive tasks led to a slower, more variable and less smooth gait pattern. These findings suggest that visuospatial processing might share common networks with locomotor control, further supporting the hypothesis that gait changes during dual task paradigms are not simply due to limited attentional resources but to competition for common networks for spatial information encoding.     

Increased attention to spatial context increases both place field stability and spatial memory

The hippocampal formation is critical for the acquisition and consolidation of memories. When recorded in freely moving animals, hippocampal pyramidal neurons fire in a location-specific manner: they are "place" cells, comprising a hippocampal representation of the animal's environment. To explore the relationship between place cells and spatial memory, we recorded from mice in several behavioral contexts. We found that long-term stability of place cell firing fields correlates with the degree of attentional demands and that successful spatial task performance was associated with stable place fields. Furthermore, conditions that maximize place field stability greatly increase orientation to novel cues. This suggests that storage and retrieval of place cells is modulated by a top-down cognitive process resembling attention and that place cells are neural correlates of spatial memory. We propose a model whereby attention provides the requisite neuromodulatation to switch short-term homosynaptic plasticity to long-term heterosynaptic plasticity, and we implicate dopamine in this process.     

Dynamic Grouping of Hippocampal Neural Activity During Cognitive Control of Two Spatial Frames

Cognitive control is the ability to coordinate multiple streams of information to prevent confusion and select appropriate behavioral responses, especially when presented with competing alternatives. Despite its theoretical and clinical significance, the neural mechanisms of cognitive control are poorly understood. Using a two-frame place avoidance task and partial hippocampal inactivation, we confirmed that intact hippocampal function is necessary for coordinating two streams of spatial information. Rats were placed on a continuously rotating arena and trained to organize their behavior according to two concurrently relevant spatial frames: one stationary, the other rotating. We then studied how information about locations in these two spatial frames is organized in the action potential discharge of ensembles of hippocampal cells. Both streams of information were represented in neuronal discharge—place cell activity was organized according to both spatial frames, but almost all cells preferentially represented locations in one of the two spatial frames. At any given time, most coactive cells tended to represent locations in the same spatial frame, reducing the risk of interference between the two information streams. An ensemble''s preference to represent locations in one or the other spatial frame alternated within a session, but at each moment, location in the more behaviorally relevant spatial frame was more likely to be represented. This discharge organized into transient groups of coactive neurons that fired together within 25 ms to represent locations in the same spatial frame. These findings show that dynamic grouping, the transient coactivation of neural subpopulations that represent the same stream of information, can coordinate representations of concurrent information streams and avoid confusion, demonstrating neural-ensemble correlates of cognitive control in hippocampus.     

Spatial cognition and neuro-mimetic navigation: a model of hippocampal place cell activity

 A computational model of hippocampal activity during spatial cognition and navigation tasks is presented. The spatial representation in our model of the rat hippocampus is built on-line during exploration via two processing streams. An allothetic vision-based representation is built by unsupervised Hebbian learning extracting spatio-temporal properties of the environment from visual input. An idiothetic representation is learned based on internal movement-related information provided by path integration. On the level of the hippocampus, allothetic and idiothetic representations are integrated to yield a stable representation of the environment by a population of localized overlapping CA3-CA1 place fields. The hippocampal spatial representation is used as a basis for goal-oriented spatial behavior. We focus on the neural pathway connecting the hippocampus to the nucleus accumbens. Place cells drive a population of locomotor action neurons in the nucleus accumbens. Reward-based learning is applied to map place cell activity into action cell activity. The ensemble action cell activity provides navigational maps to support spatial behavior. We present experimental results obtained with a mobile Khepera robot. Received: 02 July 1999 / Accepted in revised form: 20 March 2000     

Tracking the mind's image in the brain II: transcranial magnetic stimulation reveals parietal asymmetry in visuospatial imagery

The functional relevance of brain activity during visuospatial tasks was investigated by combining functional magnetic resonance imaging with unilateral repetitive transcranial magnetic stimulation (rTMS). The cognitive tasks involved visuospatial operations on visually presented and mentally imagined material ("mental clock task"). While visuospatial operations were associated with activation of the intraparietal sulcus region bilaterally, only the group which received rTMS to the right parietal lobe showed an impairment of performance during and immediately after rTMS. This functional parietal asymmetry might indicate a capacity of the right parietal lobe to compensate for a temporary suppression of the left. This is compatible with current theories of spatial hemineglect and constitutes a constraint for models of distributed information processing in the parietal lobes.     

Hippocampal "time cells" bridge the gap in memory for discontiguous events

The hippocampus is critical to remembering the flow of events in distinct experiences and, in doing so, bridges temporal gaps between discontiguous events. Here, we report a robust hippocampal representation of sequence memories, highlighted by "time cells" that encode successive moments during an empty temporal gap between the key events, while also encoding location and ongoing behavior. Furthermore, just as most place cells "remap" when a salient spatial cue is altered, most time cells form qualitatively different representations ("retime") when the main temporal parameter is altered. Hippocampal neurons also differentially encode the key events and disambiguate different event sequences to compose unique, temporally organized representations of specific experiences. These findings suggest that hippocampal neural ensembles segment temporally organized memories much the same as they represent locations of important events in spatially defined environments.     

Cortical mechanisms of space-based and object-based attentional control

Visual attention, the mechanism by which observers select relevant or important information from scenes, can be deployed to locations in space or to spatially invariant object representations. Studies have examined both the modulatory effects of attention on the strength of extrastriate cortical representations, and the control of attention by parietal and frontal cortical circuits. Subregions of parietal and frontal cortex are transiently active when attention is voluntarily shifted between spatial locations or object representations. This transient activity may reflect an abrupt shift in the attentional set of the observer, complementing sustained signals that are thought to maintain a given attentive state.     

Multiple spotlights of attentional selection in human visual cortex

Spatially directed attention strongly enhances visual perceptual processing. The metaphor of the "spotlight" has long been used to describe spatial attention; however, there has been considerable debate as to whether spatial attention must be unitary or may be split between discrete regions of space. This question was addressed here through functional MR imaging of human subjects as they performed a task that required simultaneous attention to two briefly displayed and masked targets at locations separated by distractor stimuli. These data reveal retinotopically specific enhanced activation in striate and extrastriate visual cortical representations of the two attended stimuli and no enhancement at the intervening representation of distractor stimuli. This finding of two spotlights was obtained within a single cortical hemisphere and across the two hemispheres. This provides direct evidence that spatial attention can select, in parallel, multiple low-level perceptual representations.     

Intermediate Levels of Hippocampal Activity Appear Optimal for Associative Memory Formation

Background

It is well established that hippocampal activity is positively related to effective associative memory formation. However, in biological systems often optimal levels of activity are contrasted by both sub- and supra-optimal levels. Sub-optimal levels of hippocampal activity are commonly attributed to unsuccessful memory formation, whereas the supra-optimal levels of hippocampal activity related to unsuccessful memory formation have been rarely studied. It is still unclear under what circumstances such supra-optimal levels of hippocampal activity occur. To clarify this issue, we aimed at creating a condition, in which supra-optimal hippocampal activity is associated with encoding failure. We assumed that such supra-optimal activity occurs when task-relevant information is embedded in task-irrelevant, distracting information, which can be considered as noise.

Methodology/Principal Findings

In the present fMRI study, we probed neural correlates of associative memory formation in a full-factorial design with associative memory (subsequently remembered versus forgotten) and noise (induced by high versus low distraction) as factors. Results showed that encoding failure was associated with supra-optimal activity in the high-distraction condition and with sub-optimal activity in the low distraction condition. Thus, we revealed evidence for a bell-shape function relating hippocampal activity with associative encoding success.

Conclusions/Significance

Our findings indicate that intermediate levels of hippocampal activity are optimal while both too low and too high levels appear detrimental for associative memory formation. Supra-optimal levels of hippocampal activity seem to occur when task-irrelevant information is added to task-relevant signal. If such task-irrelevant noise is reduced adequately, hippocampal activity is lower and thus optimal for associative memory formation.     

Learning through maps: functional significance of topographic organization in primary sensory cortex.

The presence of "maps" in sensory cortex is a hallmark of the mammalian nervous system, but the functional significance of topographic organization has been called into question by physiological studies claiming that patterns of neural behavioral activity transcend topographic boundaries. This paper discusses recent behavioral and physiological studies suggesting that, when animals or human subjects learn perceptual tasks, the neural modifications associated with the learning are distributed according to the spatial arrangement of the primary sensory cortical map. Topographical cortical representations of sensory events, therefore, appear to constitute a true structural framework for information processing and plasticity.     

Sleep modulates the neural substrates of both spatial and contextual memory consolidation

It is known that sleep reshapes the neural representations that subtend the memories acquired while navigating in a virtual environment. However, navigation is not process-pure, as manifold learning components contribute to performance, notably the spatial and contextual memory constituents. In this context, it remains unclear whether post-training sleep globally promotes consolidation of all of the memory components embedded in virtual navigation, or rather favors the development of specific representations. Here, we investigated the effect of post-training sleep on the neural substrates of the consolidation of spatial and contextual memories acquired while navigating in a complex 3D, naturalistic virtual town. Using fMRI, we mapped regional cerebral activity during various tasks designed to tap either the spatial or the contextual memory component, or both, 72 h after encoding with or without sleep deprivation during the first post-training night. Behavioral performance was not dependent upon post-training sleep deprivation, neither in a natural setting that engages both spatial and contextual memory processes nor when looking more specifically at each of these memory representations. At the neuronal level however, analyses that focused on contextual memory revealed distinct correlations between performance and neuronal activity in frontal areas associated with recollection processes after post-training sleep, and in the parahippocampal gyrus associated with familiarity processes in sleep-deprived participants. Likewise, efficient spatial memory was associated with posterior cortical activity after sleep whereas it correlated with parahippocampal/medial temporal activity after sleep deprivation. Finally, variations in place-finding efficiency in a natural setting encompassing spatial and contextual elements were associated with caudate activity after post-training sleep, suggesting the automation of navigation. These data indicate that post-training sleep modulates the neural substrates of the consolidation of both the spatial and contextual memories acquired during virtual navigation.     

Impaired representation of geometric relationships in humans with damage to the hippocampal formation

The pivotal role of the hippocampus for spatial memory is well-established. However, while neurophysiological and imaging studies suggest a specialization of the hippocampus for viewpoint-independent or allocentric memory, results from human lesion studies have been less conclusive. It is currently unclear whether disproportionate impairment in allocentric memory tasks reflects impairment of cognitive functions that are not sufficiently supported by regions outside the medial temporal lobe or whether the deficits observed in some studies are due to experimental factors. Here, we have investigated whether hippocampal contributions to spatial memory depend on the spatial references that are available in a certain behavioral context. Patients with medial temporal lobe lesions affecting systematically the right hippocampal formation performed a series of three oculomotor tasks that required memory of a spatial cue either in retinal coordinates or relative to a single environmental reference across a delay of 5000 ms. Stimulus displays varied the availability of spatial references and contained no complex visuo-spatial associations. Patients showed a selective impairment in a condition that critically depended on memory of the geometric relationship between spatial cue and environmental reference. We infer that regions of the medial temporal lobe, most likely the hippocampal formation, contribute to behavior in conditions that exceed the potential of viewpoint-dependent or egocentric representations. Apparently, this already applies to short-term memory of simple geometric relationships and does not necessarily depend on task difficulty or integration of landmarks into more complex representations. Deficient memory of basic geometric relationships may represent a core deficit that contributes to impaired performance in allocentric spatial memory tasks.     

Effects of attention and emotion on face processing in the human brain: an event-related fMRI study.

We used event-related fMRI to assess whether brain responses to fearful versus neutral faces are modulated by spatial attention. Subjects performed a demanding matching task for pairs of stimuli at prespecified locations, in the presence of task-irrelevant stimuli at other locations. Faces or houses unpredictably appeared at the relevant or irrelevant locations, while the faces had either fearful or neutral expressions. Activation of fusiform gyri by faces was strongly affected by attentional condition, but the left amygdala response to fearful faces was not. Right fusiform activity was greater for fearful than neutral faces, independently of the attention effect on this region. These results reveal differential influences on face processing from attention and emotion, with the amygdala response to threat-related expressions unaffected by a manipulation of attention that strongly modulates the fusiform response to faces.     

Remapping for visual stability

Visual perception is based on both incoming sensory signals and information about ongoing actions. Recordings from single neurons have shown that corollary discharge signals can influence visual representations in parietal, frontal and extrastriate visual cortex, as well as the superior colliculus (SC). In each of these areas, visual representations are remapped in conjunction with eye movements. Remapping provides a mechanism for creating a stable, eye-centred map of salient locations. Temporal and spatial aspects of remapping are highly variable from cell to cell and area to area. Most neurons in the lateral intraparietal area remap stimulus traces, as do many neurons in closely allied areas such as the frontal eye fields the SC and extrastriate area V3A. Remapping is not purely a cortical phenomenon. Stimulus traces are remapped from one hemifield to the other even when direct cortico-cortical connections are removed. The neural circuitry that produces remapping is distinguished by significant plasticity, suggesting that updating of salient stimuli is fundamental for spatial stability and visuospatial behaviour. These findings provide new evidence that a unified and stable representation of visual space is constructed by redundant circuitry, comprising cortical and subcortical pathways, with a remarkable capacity for reorganization.